Abstract
Plant tissue is composed of many different types of cells. Plant cells required to withstand mechanical pressure, such as vessel elements and fibers, have a secondary cell wall consisting of polysaccharides and lignin, which strengthen the cell wall structure and stabilize the cell shape. Previous attempts to alter the properties of the cell wall have mainly focused on reducing the amount of lignin or altering its structure in order to ease its extraction from raw woody materials for the pulp and paper and biorefinery industries. In this work, we propose the in vivo modification of the cell wall structure and mechanical properties by the introduction of resilin, an elastic protein that is able to crosslink with lignin monomers during cell wall synthesis. The effects of resilin were studied in transgenic eucalyptus plants. The protein was detected within the cell wall and its expression led to an increase in the elastic modulus of transgenic stems. In addition, transgenic stems displayed a higher yield point and toughness, indicating that they were able to absorb more energy before breaking.
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References
Bonawitz, N. D., & Chapple, C. (2010). The genetics of lignin biosynthesis: Connecting genotype to phenotype. Annual Review of Genetics, 44, 337–363.
Chen, F., & Dixon, R. A. (2007). Lignin modification improves fermentable sugar yields for biofuel production. Nature Biotechnology, 25, 759–761.
Eudes, A., et al. (2012). Biosynthesis and incorporation of side-chain-truncated lignin monomers to reduce lignin polymerization and enhance saccharification. Plant Biotechnology Journal, 10, 609–620.
Liang, H., et al. (2008). Improved sugar release from lignocellulosic material by introducing a tyrosine-rich cell wall peptide gene in poplar. CLEAN – Soil, Air, Water, 36, 662–668.
Abramson, M., Shoseyov, O., Hirsch, S., & Shani, Z. (2013). Genetic modifications of plant cell walls to increase biomass and bioethanol production. In J. Lee (Ed.), Advanced biofuels and bioproducts. New York: Springer.
Baucher, M., Halpin, C., Petit-Conil, M., & Boerjan, W. (2003). Lignin: Genetic engineering and impact on pulping. Critical Reviews in Biochemistry and Molecular Biology, 38, 305–350.
Vanholme, R., Morreel, K., Ralph, J., & Boerjan, W. (2008). Lignin engineering. Current Opinion in Plant Biology, 11, 278–285.
Boudet, A.-M. (2007). Evolution and current status of research in phenolic compounds. Phytochemistry, 68, 2722–2735.
Ralph, J., et al. (2004). Lignins: Natural polymers from oxidative coupling of 4-hydroxyphenyl- propanoids. Phytochemistry Reviews, 3, 29–60.
Cong, F., Diehl, B. G., Hill, J. L., Brown, N. R., & Tien, M. (2013). Covalent bond formation between amino acids and lignin: Cross-coupling between proteins and lignin. Phytochemistry, 96, 449–456.
Diehl, B. G., & Brown, N. R. (2014). Lignin cross-links with cysteine- and tyrosine-containing peptides under biomimetic conditions. Journal of Agriculture and Food Chemistry, 62, 10312–10319.
Mcdougall, G. J., Stewart, D., & Morrison, I. M. (1996). Tyrosine residues enhance cross-linking of synthetic proteins into lignin-like dehydrogenation products. Phytochemistry, 41, 43–47.
Weis-Fogh, T. (1960). A rubber-like protein in insect cuticle. Journal of Experimental Biology, 37, 887–907.
Qin, G., et al. (2009). Expression, cross-linking, and characterization of recombinant chitin binding resilin. Biomacromolecules, 10, 3227–3234.
Young, D., & Bennet-Clark, H. (1995). The role of the tymbal in cicada sound production. Journal of Experimental Biology, 198, 1001–1020.
Bennet-Clark, H. C., & Lucey, E. C. A. (1967). The jump of the flea: A study of the energetics and a model of the mechanism. Journal of Experimental Biology, 47, 59–67.
Burrows, M., & Sutton, G. P. (2012). Locusts use a composite of resilin and hard cuticle as an energy store for jumping and kicking. Journal of Experimental Biology, 215, 3501–3512.
Michels, J., Vogt, J., & Gorb, S. N. (2012). Tools for crushing diatoms—Opal teeth in copepods feature a rubber-like bearing composed of resilin. Scientific Reports, 2, 1–35.
Elvin, C. M., et al. (2005). Synthesis and properties of crosslinked recombinant pro-resilin. Nature, 437, 999–1002.
Rivkin, A., et al. (2015). Bionanocomposite films from resilin-CBD bound to cellulose nanocrystals. Industrial Biotechnology, 11, 44–58.
Verker, R., Rivkin, A., Zilberman, G., & Shoseyov, O. (2014). Insertion of nano-crystalline cellulose into epoxy resin via resilin to construct a novel elastic adhesive. Cellulose, 21, 4369–4379.
Yang, F., et al. (2013). Engineering secondary cell wall deposition in plants. Plant Biotechnology Journal, 11, 325–335.
Van Acker, R., et al. (2013). Lignin biosynthesis perturbations affect secondary cell wall composition and saccharification yield in Arabidopsis thaliana. Biotechnology for Biofuels, 6, 46.
Mansfield, S. D., Kang, K.-Y., & Chapple, C. (2012). Designed for deconstruction—Poplar trees altered in cell wall lignification improve the efficacy of bioethanol production. New Phytologist, 194, 91–101.
Sanami, M., et al. (2015). Biophysical and biological characterisation of collagen/resilin-like protein composite fibres. Biomedical Materials, 10, 65005.
McGann, C. L., Levenson, E. A., & Kiick, K. L. (2013). Resilin-based hybrid hydrogels for cardiovascular tissue engineering. Macromolecules, 214, 203–213.
Hauffe, K. D., et al. (1991). A parsley 4CL-1 promoter fragment specifies complex expression patterns in transgenic tobacco. The Plant Cell, 3, 435–443.
Zhong, R., et al. (2005). Arabidopsis fragile fiber8, which encodes a putative glucuronyltransferase, is essential for normal secondary wall synthesis. Plant Cell, 17, 3390–3408.
Qin, G., et al. (2011). Recombinant exon-encoded resilins for elastomeric biomaterials. Biomaterials, 32, 9231–9243.
Shani, Z., Dekel, M., Tsabary, G., & Shoseyov, O. (1997). Cloning and characterization of elongation specific endo-1,4-β-glucanase (cel1) from Arabidopsis thaliana. Plant Molecular Biology, 34, 837–842.
Carrillo, F., et al. (2005). Nanoindentation of polydimethylsiloxane elastomers: Effect of crosslinking, work of adhesion, and fluid environment on elastic modulus. Journal of Materials Research, 20, 2820–2830.
Donaldson, L. A. (2001). Lignification and lignin topochemistry—An ultrastructural view. Phytochemistry, 57, 859–873.
Prakash, M. G., & Gurumurthi, K. (2009). Genetic transformation and regeneration of transgenic plants from precultured cotyledon and hypocotyl explants of Eucalyptus tereticornis Sm. using Agrobacterium tumefaciens. In Vitro Cellular & Developmental Biology: Plant, 45, 429–434.
Paciorek, T., Sauer, M., Balla, J., Wiśniewska, J., & Friml, J. (2006). Immunocytochemical technique for protein localization in sections of plant tissues. Nature Protocols, 1, 104–107.
Acknowledgements
This research was supported by Futuragene Ltd, Rehovot, Israel. The work was performed of the Minerva Center for Bio-hybrid Complex Systems.
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Preis, I., Abramson, M. & Shoseyov, O. The Modification of Cell Wall Properties by Expression of Recombinant Resilin in Transgenic Plants. Mol Biotechnol 60, 310–318 (2018). https://doi.org/10.1007/s12033-018-0074-7
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DOI: https://doi.org/10.1007/s12033-018-0074-7